Publications
(^ co-first author, # corresponding author)
Highlights
(For a full list see below or go to Google Scholar)
Neoadjuvant immune checkpoint blockade has shown promising clinical activity. Here, we characterized early kinetics in tumor-infiltrating and circulating immune cells in oral cancer patients treated with neoadjuvant anti-PD-1 or anti-PD-1/CTLA-4 in a clinical trial (NCT02919683). Tumor-infiltrating CD8 T cells that clonally expanded during immunotherapy expressed elevated tissue-resident memory and cytotoxicity programs, which were already active prior to therapy, supporting the capacity for rapid response. Systematic target discovery revealed that treatment-expanded tumor T cell clones in responding patients recognized several self-antigens, including the cancer-specific antigen MAGEA1. The frequency of activated blood CD8 T cells, notably pre-treatment PD-1-positive KLRG1-negative T cells, was strongly associated with intra-tumoral pathological response. These results demonstrate how neoadjuvant checkpoint blockade induces local and systemic tumor immunity.
Adrienne M. Luoma^; Shengbao Suo^#; Yifan Wang; Lauren Gunasti; Caroline B.M. Porter; Nancy Nabilsi; Jenny Tadros; Andrew P. Ferretti; Sida Liao; Cagan Gurer; Yu-Hui Chen; Shana Criscitiello; Cora A. Ricker; Danielle Dionne; Orit Rozenblatt-Rosen; Ravindra Uppaluri; Robert I. Haddad; Orr Ashenberg; Aviv Regev; Eliezer M. Van Allen; Gavin MacBeath; Jonathan D. Schoenfeld#; Kai W. Wucherpfennig#
Checkpoint blockade with antibodies specific for the PD-1 and CTLA-4 inhibitory receptors can induce durable responses in a wide range of human cancers. However, the immunological mechanisms responsible for severe inflammatory side effects remain poorly understood. Here we report a comprehensive single-cell analysis of immune cell populations in colitis, a common and severe side effect of checkpoint blockade. We observed a striking accumulation of CD8 T cells with highly cytotoxic and proliferative states and no evidence of regulatory T cell depletion. T cell receptor (TCR) sequence analysis demonstrated that a substantial fraction of colitis-associated CD8 T cells originated from tissue-resident populations, explaining the frequently early onset of colitis symptoms following treatment initiation. Our analysis also identified cytokines, chemokines, and surface receptors that could serve as therapeutic targets for colitis and potentially other inflammatory side effects of checkpoint blockade.
Adrienne M. Luoma^; Shengbao Suo^; Hannah L. Williams; Tatyana Sharova; Keri Sullivan; Michael Manos; Peter Bowling; F. Stephen Hodi; Osama Rahma; Ryan J. Sullivan; Genevieve M. Boland; Jonathan A. Nowak; Stephanie K. Dougan; Michael Dougan#; Guo-Cheng Yuan; Kai W. Wucherpfennig#
Full List
Three-dimensional molecular architecture of mouse organogenesis
Fangfang Qu^; Wenjia Li^; Jian Xu^; Ruifang Zhang; Jincan Ke; Xiaodie Ren; Xiaogao Meng; Lexin Qin; Jingna Zhang; Fangru Lu; Xin Zhou; Xi Luo; Zhen Zhang; Minhan Wang; Guangming Wu; Duanqing Pei; Jiekai Chen; Guizhong Cui#; Shengbao Suo#; Guangdun Peng#
Nature Communications, 2023, 14:4599
Construction of a cross-species cell landscape at single-cell level
Renying Wang^; Peijing Zhang^#; Jingjing Wang^; Lifeng Ma^; Weigao E^; ShengBao Suo^; Mengmeng Jiang^; Jiaqi Li^; Haide Chen; Huiyu Sun; Lijiang Fei; Ziming Zhou; Yincong Zhou; Yao Chen; Weiqi Zhang; Xinru Wang; Yuqing Mei; Zhongyi Sun; Chengxuan Yu; Jikai Shao; Yuting Fu; Yanyu Xiao; Fang Ye; Xing Fang; Hanyu Wu; Qile Guo; Xiunan Fang; Xia Li; Xianzhi Gao; Dan Wang; Peng-Fei Xu; Rui Zeng; Gang Xu; Lijun Zhu; Lie Wang; Jing Qu; Dan Zhang; Hongwei Ouyang; He Huang; Ming Chen; Shyh-Chang NG#; Guang-Hui Liu#; Guo-Cheng Yuan#; Guoji Guo#; Xiaoping Han#
Nucleic Acids Research, 2023, 51(2):501-516
Tissue-resident memory and circulating T cells are early responders to pre-surgical cancer immunotherapy
Adrienne M. Luoma^; Shengbao Suo^#; Yifan Wang; Lauren Gunasti; Caroline B.M. Porter; Nancy Nabilsi; Jenny Tadros; Andrew P. Ferretti; Sida Liao; Cagan Gurer; Yu-Hui Chen; Shana Criscitiello; Cora A. Ricker; Danielle Dionne; Orit Rozenblatt-Rosen; Ravindra Uppaluri; Robert I. Haddad; Orr Ashenberg; Aviv Regev; Eliezer M. Van Allen; Gavin MacBeath; Jonathan D. Schoenfeld#; Kai W. Wucherpfennig#
Cell, 2022, 185(16):2918-2935
Molecular pathways of colon inflammation induced by cancer immunotherapy
Adrienne M. Luoma^; Shengbao Suo^; Hannah L. Williams; Tatyana Sharova; Keri Sullivan; Michael Manos; Peter Bowling; F. Stephen Hodi; Osama Rahma; Ryan J. Sullivan; Genevieve M. Boland; Jonathan A. Nowak; Stephanie K. Dougan; Michael Dougan#; Guo-Cheng Yuan; Kai W. Wucherpfennig#
Cell, 2020, 182(3):655-671
Molecular architecture of lineage allocation and tissue organization in early mouse embryo
Guangdun Peng^#; Shengbao Suo^; Guizhong Cui^; Fang Yu^; Ran Wang; Jun Chen; Shirui Chen; Zhiwen Liu; Guoyu Chen; Yun Qian; Patrick P.L.Tam; Jing-Dong J.Han#; Naihe Jing#
Nature, 2019, 572(7770):528-532
Revealing the critical regulators of cell identity in the mouse cell atlas
Shengbao Suo; Qian Zhu; Assieh Saadatpour; Lijiang Fei; Guoji Guo; Guo-Cheng Yuan#
Cell Reports, 2018, 6(25):1436-1445
Spatial transcriptomic analysis of cryosectioned tissue samples with Geo-seq
Jun Chen^; Shengbao Suo^; Patrick PL Tam; Jing-Dong J Han#; Guangdun Peng#; Naihe Jing#
Nature Protocols, 2017, 12(3):566-580
Spatial transcriptome for the molecular annotation of lineage fates and cell identity in mid-gastrula mouse embryo
Guangdun Peng^; Shengbao Suo^; Jun Chen^; Weiyang Chen; Chang Liu; Fang Yu; Ran Wang; Shirui Chen; Na Sun; Guizhong Cui; Lu Song; Patrick P.L. Tam; Jing-Dong J.Han#; Naihe Jing#
Developmental Cell, 2016, 36(6):681-697
Mouse gastrulation:Attributes of transcription factor regulatory network for epiblast patterning
Guizhong Cui^; Shengbao Suo^; Ran Wang; Yun Qian; Jing-Dong J. Han#; Guangdun Peng#; Patrick P. L. Tam#; Naihe Jing#
Development, Growth & Differentiation, 2018, 60(8):463-472
PSEA:Kinase-specific prediction and analysis of human phosphorylation substrates
Sheng-Bao Suo; Jian-Ding Qiu#; Shao-Ping Shi; Xiang Chen; Ru-Ping Liang
Scientific Reports, 2014, 4(4):4524
Proteome-wide analysis of amino acid variations that influences protein lysine acetylation
Sheng-Bao Suo; Jian-Ding Qiu#; Shao-Ping Shi; Xiang Chen; Shu-Yun Huang; Ru-Ping Liang
Journal of Proteome Research, 2013, 12 (2):949-958
Position-Specific Analysis and Prediction for Protein Lysine Acetylation Based on Multiple Features
Sheng-Bao Suo; Jian-Ding Qiu#; Shao-Ping Shi; Xing-Yu Sun; Shu-Yun Huang; Xiang Chen; Ru-Ping Liang
PLoS ONE, 2012, 7( 11):e49108
Single-nucleus transcriptome analysis of human brain immune response in patients with severe COVID-19
John F Fullard, Hao-Chih Lee, Georgios Voloudakis, Shengbao Suo, Behnam Javidfar, Zhiping Shao, Cyril Peter, Wen Zhang, Shan Jiang, André Corvelo, Heather Wargnier, Emma Woodoff-Leith, Dushyant P Purohit, Sadhna Ahuja, Nadejda M Tsankova, Nathalie Jette, Gabriel E Hoffman, Schahram Akbarian, Mary Fowkes, John F Crary, Guo-Cheng Yuan, Panos Roussos
Genome Medicine, 2021, 13(1):118
Massively parallel in vivo CRISPR screening identifies RNF20/40 as epigenetic regulators of cardiomyocyte maturation
Nathan J VanDusen, Julianna Y Lee, Weiliang Gu, Catalina E Butler, Isha Sethi, Yanjiang Zheng, Justin S King, Pingzhu Zhou, Shengbao Suo, Yuxuan Guo, Qing Ma, Guo-Cheng Yuan, William William Pu
Nature Communications, 2021, 12(1):4442
Immunosuppressive Myeloid Cells Induce Nitric Oxide–Dependent DNA Damage and p53 Pathway Activation in CD8+ T Cells
Adam NR Cartwright, Shengbao Suo, Soumya Badrinath, Sushil Kumar, Johannes Melms, Adrienne Luoma, Archis Bagati, Assieh Saadatpour, Benjamin Izar, Guo-Cheng Yuan, Kai W Wucherpfennig#
Cancer Immunology Research, 2021, 9(4):470-485
New regulators of Drosophila eye development identified from temporal transcriptome changes
Manon Quiquand, Gerard Rimesso, Nan Qiao, Shengbao Suo, Chunyu Zhao, Matthew Slattery, Kevin P White, Jackie J Han, Nicholas E Baker#
Genetics, 2021, 217(4):iyab007
Inhibition of CDK4/6 promotes CD8 T-cell memory formation
Max Heckler, Lestat R Ali, Eleanor Clancy-Thompson, Li Qiang, Katherine S Ventre, Patrick Lenehan, Kevin Roehle, Adrienne Luoma, Kelly Boelaars, Vera Peters, Julia McCreary, Tamara Boschert, Eric S Wang, Shengbao Suo, Francesco Marangoni, Thorsten R Mempel, Henry W Long, Kai W Wucherpfennig, Michael Dougan, Nathanael S Gray, Guo-Cheng Yuan, Shom Goel, Sara M Tolaney, Stephanie K Dougan#
Cancer Discovery, 2021, candisc.1540.2020
Integrated spatial genomics reveals global architecture of single nuclei
Yodai Takei; Jina Yun; Shiwei Zheng; Noah Ollikainen; Nico Pierson; Jonathan White; Sheel Shah; Julian Thomassie; Shengbao Suo; Chee-Huat Linus Eng; Mitchell Guttman; Guo-Cheng Yuan; Long Cai#
Nature, 2021, 590(7845):344-350
Transcriptional network dynamics during the progression of pluripotency revealed by integrative statistical learning
Hani Jieun Kim; Pierre Osteil; Sean J Humphrey; Senthilkumar Cinghu; Andrew J Oldfield; Ellis Patrick; Emilie E Wilkie; Guangdun Peng; Shengbao Suo; Raja Jothi; Patrick P L Tam; Pengyi Yang#
Nucleic Acids Research, 2019, 48(4):1828-1842
A 3D Atlas of Hematopoietic Stem and Progenitor Cell Expansion by Multi-dimensional RNA-Seq Analysis
Yuanyuan Xue^; Denghui Liu^; Guizhong Cui; Yanyan Ding; Daosheng Ai; Suwei Gao; Yifan Zhang; Shengbao Suo; Xiaohan Wang; Peng Lv; Chunyu Zhou; Yizhou Li; Xingwei Chen; Guangdun Peng; Naihe Jing; Jing-Dong J.Han#; Feng Liu#
Cell Reports, 2019, 27(5):1567-1578
Epithelial endoplasmic reticulum stress orchestrates a protective IgA response
Joep Grootjans^; Niklas Krupka^; Shuhei Hosomi^; Juan D.Matute; Thomas Hanley; Svetlana Saveljeva; Thomas Gensollen; Jarom Heijmans; Hai Li; Julien P.Limenitakis; Stephanie C.Ganal-Vonarburg; Shengbao Suo; Adrienne M. Luoma; Yosuke Shimodaira; Jinzhi Duan; David Q.Shih; Margaret E.Conner; Jonathan N.Glickman; Gwenny M.Fuhler; Noah W.Palm; Marcel R.de Zoete; C. Janneke van der Woude; Guo-Cheng Yuan; Kai W.Wucherpfennig; Stephan R. Targan; Philip Rosenstiel; Richard A.Flavell; Kathy D.McCoy; Andrew J. Macpherson; Arthur Kaser; Richard S.Blumberg#
Science, 2019, 363(6 430):993-998
Accurate drug repositioning through non- tissue-specific core signatures from cancer transcriptomes
Chi Xu^; Daosheng Ai^; Dawei Shi; Shengbao Suo; Xingwei Chen; Yizhen Yan; Yaqiang Cao; Na Sun; Weizhong Chen; Joseph McDermott; Shiqiang Zhang; Yingying Zeng; Jing-Dong J. Han#
Cell Reports, 2018 , 25(2):523-535
Single-cell transcriptomic analysis of cardiac differentiation from human PSCs reveals HOPX-dependent cardiomyocyte maturation
Clayton E. Friedman^; Quan Nguyen^; Samuel W. Lukowski^; Abbigail Helfer; Han Sheng Chiu; Jason Miklas; Shiri Levy; Shengbao Suo; Jing-Dong Jackie Han; Pierre Osteil; Guangdun Peng; Naihe Jing; Greg J. Baillie; Anne Senabouth; Angelika N. Christ; Timothy J. Bruxner; Charles E. Murry; Emily S. Wong; Jun Ding; Joseph E. Powell#; Nathan J. Palpant#
Cell Stem Cell, 2018, 23(4):586- 598
Inference of differentiation time for single cell transcriptomes using cell population reference data
Na Sun^; Xiaoming Yu^; Fang Li^; Denghui Liu; Shengbao Suo; Weiyang Chen; Shirui Chen; Lu Song; Christopher D. Green; Joseph McDermott; Qin Shen; Naihe Jing; Jing-Dong J. Han#
Nature Communications, 2017, 8:1856-1856
Transcriptome analyses of rhesus monkey preimplantation embryos reveal a reduced capacity for DNA double-strand break repair in primate oocytes and early embryos
Xinyi Wang^; Denghui Liu^; Dajian He; Shengbao Suo; Xian Xia; Xiechao He; Jing-Dong J. Han#; Ping Zheng#
Genome Research, 2017, 27( 4):567-579
Nkx2.5 marks angioblasts that contribute to hemogenic endothelium of the endocardium and dorsal aorta
Lyad Zamir^; Reena Singh^; Elisha Nathan; Ralph Patrick; Oren Yifa; Yfat Yahalom-Ronen; Alaa A Arraf; Thomas M Schultheiss; Shengbao Suo; Jing- Dong Jackie Han; Guangdun Peng; Naihe Jing; Yuliang Wang; Nathan Palpant; Patrick PL Tam; Richard P Harvey#; Eldad Tzahor#
eLife, 2017, 6:e20994
A homology-based pipeline for global prediction of post-translational modification sites
Xiang Chen; Shao-Ping Shi; Hao-Dong Xu; Sheng-Bao Suo; Jian-Ding Qiu#
Scientific Reports, 2016, 6:25801
Proteomic analysis and prediction of human phosphorylation sites in subcellular level reveal subcellular specificity
Xiang Chen; Shao-Ping Shi; Sheng-Bao Suo; Hao-Dong Xu; Jian-Ding Qiu#
Bioinformatics, 2015, 31(2):194-200
Systematic analysis and prediction of pupylation sites in prokaryotic proteins
Xiang Chen; Jian-Ding Qiu#; Shao-Ping Shi; Sheng-Bao Suo; Ru-Ping Liang
PLoS ONE, 2013, 8(9):e74002
Incorporating key position and amino acid residue features to identify general and species-specific Ubiquitin conjugation sites
Xiang Chen; Jian-Ding Qiu#; Shao-Ping Shi; Sheng-Bao Suo; Shu-Yun Huang; Ru-Ping Liang
Bioinformatics, 2013, 29(13):1614-1622
The prediction of palmitoylation site locations using a multiple feature extraction method
Shao-Ping Shi; Xing-Yu Sun; Jian-Ding Qiu#; Sheng-Bao Suo; Xiang Chen; Shu-Yun Huang; Ru-Ping Liang
Journal of Molecular Graphics & Modelling, 2013, 40:125-130
A method to distinguish between lysine acetylation and lysine methylation from protein sequences
Shao-Ping Shi; Jian-Ding Qiu#; Xing-Yu Sun; Sheng-Bao Suo; Shu-Yun Huang; Ru-Ping Liang
Journal of Theoretical Biology, 20 12, 310:223-230
PredSulSite:Prediction of protein tyrosine sulfation sites with multiple features and analysis
Shu-Yun Huang; Shao-Ping Shi; Jian-Ding Qiu#; Xing-Yu Sun; Sheng-Bao Suo; Ru-Ping Liang
Analytical Biochemistry, 2012, 428 (1):16-23
PMeS:Prediction of methylation sites based on enhanced feature encoding scheme
Shao-Ping Shi; Jian-Ding Qiu#; Xing-Yu Sun; Sheng-Bao Suo; Shu-Yun Huang; Ru-Ping Liang
PLoS ONE, 2012, 7(6):e38772
A novel algorithm combining support vector machine with the discrete wavelet transform for the prediction of protein subcellular localization
Ru-Ping Liang; Shu-Yun Huang; Shao-Ping Shi; Xing-Yu Sun; Sheng-Bao Suo; Jian-Ding Qiu#
Computers in Biology and Medicine, 2012, 42(2):180-187
Identifying protein quaternary structural attributes by incorporating physicochemical properties into the general form of Chou’s PseAAC via discrete wavelet transform
Xing-Yu Sun; Shao-Ping Shi; Jian-Ding Qiu#; Sheng-Bao Suo; Shu-Yun Huang; Ru-Ping Liang
Molecular BioSystems, 2012, 8(12):3178-3184
PLMLA:prediction of lysine methylation and lysine acetylation by combining multiple features
Shao-Ping Shi; Jian-Ding Qiu#; Xing-Yu Sun; Sheng-Bao Suo; Shu-Yun Huang; Ru-Ping Liang
Molecular BioSystems, 2012, 8(5):1520-1527
OligoPred:A web-server for predicting homo-oligomeric proteins by incorporating discrete wavelet transform into Chou’s pseudo amino acid composition
Jian-Ding Qiu#; Sheng-Bao Suo; Xing-Yu Sun; Shao-Ping Shi; Ru-Ping Liang
Journal of Molecular Graphics & Modelling, 2011, 30:129-134
Predicting homo-oligomers and hetero-oligomers by pseudo-amino acid composition An approach from discrete wavelet transformation
Jian-Ding Qiu#; Xing-Yu Sun; Sheng-Bao Suo; Shao-Ping Shi; Shu-Yun Huang; Ru-Ping Liang; Li Zhang
Biochimie, 2011, 93(7):1132-1138
Identify submitochondria and subchloroplast locations with pseudo amino acid composition Approach from the strategy of discrete wavelet transform feature extraction
Shao-Ping Shi; Jian-Ding Qiu#; Xing-Yu Sun; Jian-Hua Huang; Shu-Yun Huang; Sheng-Bao Suo; Ru-Ping Liang; Li Zhang
Biochimica et Biophysica Acta - Molecular Cell Research, 2011, 1813(3):424-430